Pathophysiology of mitochondrial disease causing epilepsy and status epilepticus

Epilepsy and Behavior

Volumn 49, Issue , 2015, Pages 71-75

  Rahman, Shamima ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b GREAT ORMOND STREET HOSPITAL   (United Kingdom)

Author keywords

Calcium homeostasis and signaling; Cerebral folate deficiency; Coenzyme Q10; Epilepsy; Immune dysfunction; L arginine; Mitochondrial disease; Neuronal energy depletion; Oxidative stress; Seizure

Indexed keywords

5,10 METHYLENETETRAHYDROFOLATE REDUCTASE (FADH2); ADENOSINE TRIPHOSPHATE; ARGININE; ASCORBIC ACID; CALCIUM; CITRULLINE; FOLIC ACID; GLUTAMATE TRANSPORTER; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UBIDECARENONE;

BRAIN DISEASE; BRAIN MITOCHONDRION; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CELL FUNCTION; CEREBRAL FOLATE DEFICIENCY; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME SYNTHESIS; EPILEPSY; EPILEPTIC STATE; EPILEPTOGENESIS; GENE MUTATION; GENETIC ASSOCIATION; HUMAN; IMMUNE RESPONSE; KEARNS SAYRE SYNDROME; MELAS SYNDROME; MERRF SYNDROME; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; REVIEW; ANIMAL; ASTROCYTE; BRAIN; COMPLICATION; MITOCHONDRION; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; STATUS EPILEPTICUS;

ANIMALS; ASTROCYTES; BRAIN; EPILEPSY; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; NEURONS; OXIDATIVE STRESS; STATUS EPILEPTICUS;

EID: 84938979769     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2015.05.003     Document Type: Review

References (55)

1. Simeone K.A., Matthews S.A., Samson K.K., Simeone T.A. Targeting deficiencies in mitochondrial respiratory complex I and functional uncoupling exerts anti-seizure effects in a genetic model of temporal lobe epilepsy and in a model of acute temporal lobe seizures. Exp Neurol 2014, 251:84-90.
2. Rowley S., Liang L.P., Fulton R., Shimizu T., Day B., Patel M. Mitochondrial respiration deficits driven by reactive oxygen species in experimental temporal lobe epilepsy. Neurobiol Dis 2015, 75:151-158.
3. Steinlein O.K. Calcium signaling and epilepsy. Cell Tissue Res 2014, 357:385-393.
4. Rahman S. Mitochondrial disease and epilepsy. Dev Med Child Neurol 2012, 54:397-406.
5. Kann O., Kovacs R. Mitochondria and neuronal activity. Am J Physiol Cell Physiol 2007, 292:C641-C657.
6. Munnich A., Rotig A., Chretien D., Cormier V., Bourgeron T., Bonnefont J.P., et al. Clinical presentation of mitochondrial disorders in childhood. J Inherit Metab Dis 1996, 19:521-527.
7. Debray F.G., Lambert M., Chevalier I., Robitaille Y., Decarie J.C., Shoubridge E.A., et al. Long-term outcome and clinical spectrum of 73 pediatric patients with mitochondrial diseases. Pediatrics 2007, 119:722-733.
8. El Sabbagh S., Lebre A.S., Bahi-Buisson N., Delonlay P., Soufflet C., Boddaert N., et al. Epileptic phenotypes in children with respiratory chain disorders. Epilepsia 2010, 51:1225-1235.
9. Goto Y., Nonaka I., Horai S. A mutation in the tRNA(Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature 1990, 348:651-653.
10. Shoffner J.M., Lott M.T., Lezza A.M., Seibel P., Ballinger S.W., Wallace D.C. Myoclonic epilepsy and ragged-red fiber disease (MERRF) is associated with a mitochondrial DNA tRNA(Lys) mutation. Cell 1990, 61:931-937.
11. Liolitsa D., Rahman S., Benton S., Carr L.J., Hanna M.G. Is the mitochondrial complex I ND5 gene a hot-spot for MELAS causing mutations?. Ann Neurol 2003, 53:128-132.
12. Thorburn D.R., Rahman S.M. GeneReviews(r) [Internet] 1993-2015, 2003 Oct 30 [updated 2014 Apr 17], Seattle (WA): University of Washington, Seattle, Available from http://www.ncbi.nlm.nih.gov/books/NBK1173/PubMed PMID: 20301352. R.A. Pagon, M.P. Adam, H.H. Ardinger, S.E. Wallace, A. Amemiya, L.J.H. Bean, T.D. Bird, C.R. Dolan, C.T. Fong, R.J.H. Smith, K. Stephens (Eds.).
13. Desguerre I., Pinton F., Nabbout R., Moutard M.L., N'Guyen S., Marsac C., et al. Infantile spasms with basal ganglia MRI hypersignal may reveal mitochondrial disorder due to T8993G MT DNA mutation. Neuropediatrics 2003, 34:265-269.
14. Patel M.N. Oxidative stress, mitochondrial dysfunction, and epilepsy. Free Radic Res 2002, 36:1139-1146.
15. Jacobson J., Duchen M.R., Hothersall J., Clark J.B., Heales S.J. Induction of mitochondrial oxidative stress in astrocytes by nitric oxide precedes disruption of energy metabolism. J Neurochem 2005, 95:388-395.
16. Liang L.P., Patel M. Mitochondrial oxidative stress and increased seizure susceptibility in Sod2(-/+) mice. Free Radic Biol Med 2004, 36:542-554.
17. Ferdinandusse S., Waterham H.R., Heales S.J., Brown G.K., Hargreaves I.P., Taanman J.W., et al. HIBCH mutations can cause Leigh-like disease with combined deficiency of multiple mitochondrial respiratory chain enzymes and pyruvate dehydrogenase. Orphanet J Rare Dis 2013, 8:188.
18. Kovac S., Domijan A.M., Walker M.C., Abramov A.Y. Seizure activity results in calcium- and mitochondria-independent ROS production via NADPH and xanthine oxidase activation. Cell Death Dis 2014, 5:e1442.
19. Llorente-Folch I., Rueda C.B., Pardo B., Szabadkai G., Duchen M.R., Satrustegui J. The regulation of neuronal mitochondrial metabolism by calcium. J Physiol 2015.
20. Kunz W.S. The role of mitochondria in epileptogenesis. Curr Opin Neurol 2002, 15:179-184.
21. Sancak Y., Markhard A.L., Kitami T., Kovacs-Bogdan E., Kamer K.J., Udeshi N.D., et al. EMRE is an essential component of the mitochondrial calcium uniporter complex. Science 2013, 342:1379-1382.
22. Logan C.V., Szabadkai G., Sharpe J.A., Parry D.A., Torelli S., Childs A.M., et al. Loss-of-function mutations in MICU1 cause a brain and muscle disorder linked to primary alterations in mitochondrial calcium signaling. Nat Genet 2014, 46:188-193.
23. Niespodziany I., Klitgaard H., Margineanu D.G. Levetiracetam inhibits the high-voltage-activated Ca(2+) current in pyramidal neurones of rat hippocampal slices. Neurosci Lett 2001, 306:5-8.
24. Mancuso M., Galli R., Pizzanelli C., Filosto M., Siciliano G., Murri L. Antimyoclonic effect of levetiracetam in MERRF syndrome. J Neurol Sci 2006, 243:97-99.
25. Neeve V.C., Samuels D.C., Bindoff L.A., van den Bosch B., Van GG Smeets H., et al. What is influencing the phenotype of the common homozygous polymerase-gamma mutation p.Ala467Thr?. Brain 2012, 135:3614-3626.
26. Hasselmann O., Blau N., Ramaekers V.T., Quadros E.V., Sequeira J.M., Weissert M. Cerebral folate deficiency and CNS inflammatory markers in Alpers disease. Mol Genet Metab 2010, 99:58-61.
27. Harris M.O., Walsh L.E., Hattab E.M., Golomb M.R. Is it ADEM, POLG, or both?. Arch Neurol 2010, 67:493-496.
28. Al-Zubeidi D., Thangarajh M., Pathak S., Cai C., Schlaggar B.L., Storch G.A., et al. Fatal human herpesvirus 6-associated encephalitis in two boys with underlying POLG mitochondrial disorders. Pediatr Neurol 2014, 51:448-452.
29. Fassone E., Taanman J.W., Hargreaves I.P., Sebire N.J., Cleary M.A., Burch M., et al. Mutations in the mitochondrial complex I assembly factor NDUFAF1 cause fatal infantile hypertrophic cardiomyopathy. J Med Genet 2011, 48:691-697.
30. Pardo C.A., Nabbout R., Galanopoulou A.S. Mechanisms of epileptogenesis in pediatric epileptic syndromes: Rasmussen encephalitis, infantile spasms, and febrile infection-related epilepsy syndrome (FIRES). Neurotherapeutics 2014, 11:297-310.
31. Pineda M., Ormazabal A., Lopez-Gallardo E., Nascimento A., Solano A., Herrero M.D., et al. Cerebral folate deficiency and leukoencephalopathy caused by a mitochondrial DNA deletion. Ann Neurol 2006, 59:394-398.
32. Spector R., Johanson C.E. Choroid plexus failure in the Kearns-Sayre syndrome. Cerebrospinal Fluid Res 2010, 7:14.
33. Rahman S., Footitt E.J., Varadkar S., Clayton P.T. Inborn errors of metabolism causing epilepsy. Dev Med Child Neurol 2013, 55:23-36.
34. Quijada-Fraile P., Callaghan O., Martin-Hernandez E., Montero R., Garcia-Cazorla A., de A.A., et al. Follow-up of folinic acid supplementation for patients with cerebral folate deficiency and Kearns-Sayre syndrome. Orphanet J Rare Dis 2014, 9:3.
35. Rahman S., Clarke C.F., Hirano M. 176th ENMC International Workshop: diagnosis and treatment of coenzyme Q(10) deficiency. Neuromuscul Disord 2012, 22:76-86.
36. Brea-Calvo G., Haack T.B., Karall D., Ohtake A., Invernizzi F., Carrozzo R., et al. COQ4 mutations cause a broad spectrum of mitochondrial disorders associated with CoQ10 deficiency. Am J Hum Genet 2015, 96:309-317.
37. Desbats M.A., Lunardi G., Doimo M., Trevisson E., Salviati L. Genetic bases and clinical manifestations of coenzyme Q10 (CoQ 10) deficiency. J Inherit Metab Dis 2015, 38:145-156.
38. Lagier-Tourenne C., Tazir M., Lopez L.C., Quinzii C.M., Assoum M., Drouot N., et al. ADCK3, an ancestral kinase, is mutated in a form of recessive ataxia associated with coenzyme Q10 deficiency. Am J Hum Genet 2008, 82:661-672.
39. Mollet J., Delahodde A., Serre V., Chretien D., Schlemmer D., Lombes A., et al. CABC1 gene mutations cause ubiquinone deficiency with cerebellar ataxia and seizures. Am J Hum Genet 2008, 82:623-630.
40. Heeringa S.F., Chernin G., Chaki M., Zhou W., Sloan A.J., Ji Z., et al. COQ6 mutations in human patients produce nephrotic syndrome with sensorineural deafness. J Clin Invest 2011, 121:2013-2024.
41. Rahman S., Hargreaves I., Clayton P., Heales S. Neonatal presentation of coenzyme Q10 deficiency. J Pediatr 2001, 139:456-458.
42. Duncan A.J., Bitner-Glindzicz M., Meunier B., Costello H., Hargreaves I.P., Lopez L.C., et al. A nonsense mutation in COQ9 causes autosomal-recessive neonatal-onset primary coenzyme Q10 deficiency: a potentially treatable form of mitochondrial disease. Am J Hum Genet 2009, 84:558-566.
43. Cohen R., Basel-Vanagaite L., Goldberg-Stern H., Halevy A., Shuper A., Feingold-Zadok M., et al. Two siblings with early infantile myoclonic encephalopathy due to mutation in the gene encoding mitochondrial glutamate/H+ symporter SLC25A22. Eur J Paediatr Neurol 2014, 18:801-805.
44. Molinari F., Kaminska A., Fiermonte G., Boddaert N., Raas-Rothschild A., Plouin P., et al. Mutations in the mitochondrial glutamate carrier SLC25A22 in neonatal epileptic encephalopathy with suppression bursts. Clin Genet 2009, 76:188-194.
45. Molinari F., Raas-Rothschild A., Rio M., Fiermonte G., Encha-Razavi F., Palmieri L., et al. Impaired mitochondrial glutamate transport in autosomal recessive neonatal myoclonic epilepsy. Am J Hum Genet 2005, 76:334-339.
46. Poduri A., Heinzen E.L., Chitsazzadeh V., Lasorsa F.M., Elhosary P.C., LaCoursiere C.M., et al. SLC25A22 is a novel gene for migrating partial seizures in infancy. Ann Neurol 2013, 74:873-882.
47. Falk M.J., Li D., Gai X., McCormick E., Place E., Lasorsa F.M., et al. AGC1 deficiency causes infantile epilepsy, abnormal myelination, and reduced N-acetylaspartate. JIMD Rep 2014, 14:77-85.
48. Wibom R., Lasorsa F.M., Tohonen V., Barbaro M., Sterky F.H., Kucinski T., et al. AGC1 deficiency associated with global cerebral hypomyelination. N Engl J Med 2009, 361:489-495.
49. Koga Y., Povalko N., Nishioka J., Katayama K., Kakimoto N., Matsuishi T. MELAS and l-arginine therapy: pathophysiology of stroke-like episodes. Ann N Y Acad Sci 2010, 1201:104-110.
50. Naini A., Kaufmann P., Shanske S., Engelstad K., De Vivo D.C., Schon E.A. Hypocitrullinemia in patients with MELAS: an insight into the "MELAS paradox". J Neurol Sci 2005, 229-230:187-193.
51. El-Hattab A.W., Hsu J.W., Emrick L.T., Wong L.J., Craigen W.J., Jahoor F., et al. Restoration of impaired nitric oxide production in MELAS syndrome with citrulline and arginine supplementation. Mol Genet Metab 2012, 105:607-614.
52. Debray F.G., Lambert M., Allard P., Mitchell G.A. Low citrulline in Leigh disease: still a biomarker of maternally inherited Leigh syndrome. J Child Neurol 2010, 25:1000-1002.
53. Lightowlers R.N., Chrzanowska-Lightowlers Z.M. Salvaging hope: is increasing NAD(+) a key to treating mitochondrial myopathy?. EMBO Mol Med 2014, 6:705-707.
54. Cerutti R., Pirinen E., Lamperti C., Marchet S., Sauve A.A., Li W., et al. NAD(+)-dependent activation of Sirt1 corrects the phenotype in a mouse model of mitochondrial disease. Cell Metab 2014, 19:1042-1049.
55. Khan N.A., Auranen M., Paetau I., Pirinen E., Euro L., Forsstrom S., et al. Effective treatment of mitochondrial myopathy by nicotinamide riboside, a vitamin B3. EMBO Mol Med 2014, 6:721-731.